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Frontiers in Zoology Biomed Central Frontiers in Zoology BioMed Central Research Open Access A novel and ancient group of type I keratins with members in bichir, sturgeon and gar Michael Schaffeld*1, Mark Haberkamp1, Sonja Schätzlein2, Sebastian Neumann1 and Christian Hunzinger3 Address: 1Institute of Zoology, Johannes-von-Müller-Weg 6, Johannes Gutenberg University, D-55099 Mainz, Germany, 2Dept. of Gastroenterology, Medical School Hannover, Carl Neuberg Str. 1, K11, E01, R1400, 30629 Hannover, Germany and 3Merck KGaA, Central Services Analytics, Central Product Analytics/Bioanalytics, Frankfurter Str. 250, D-64293 Darmstadt, Germany Email: Michael Schaffeld* - [email protected]; Mark Haberkamp - [email protected]; Sonja Schätzlein - schaetzlein.sonja@mh- hannover.de; Sebastian Neumann - [email protected]; Christian Hunzinger - [email protected] * Corresponding author Published: 6 June 2007 Received: 22 December 2006 Accepted: 6 June 2007 Frontiers in Zoology 2007, 4:16 doi:10.1186/1742-9994-4-16 This article is available from: http://www.frontiersinzoology.com/content/4/1/16 © 2007 Schaffeld et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract 1. Background: Vertebrate epithelial cells typically express a specific set of keratins. In teleosts, keratins are also present in a variety of mesenchymal cells, which usually express vimentin. Significantly, our previous studies revealed that virtually all known teleost keratins evolved independently from those present in terrestrial vertebrates. To further elucidate the evolutionary scenario that led to the large variety of keratins and their complex expression patterns in present day teleosts, we have investigated their presence in bichir, sturgeon and gar. 2. Results: We have discovered a novel group of type I keratins with members in all three of these ancient ray-finned fish, but apparently no counterparts are present in any other vertebrate class so far investigated, including the modern teleost fish. From sturgeon and gar we sequenced one and from bichir two members of this novel keratin group. By complementary keratin blot-binding assays and peptide mass fingerprinting using MALDI-TOF mass spectrometry, in sturgeon we were able to assign the sequence to a prominent protein spot, present exclusively in a two-dimensionally separated cytoskeletal preparation of skin, thus identifying it as an epidermally expressed type I keratin. In contrast to the other keratins we have so far sequenced from bichir, sturgeon and gar, these new sequences occupy a rather basal position within the phylogenetic tree of type I keratins, in a close vicinity to the keratins we previously cloned from river lamprey. 3. Conclusion: Thus, this new K14 group seem to belong to a very ancient keratin branch, whose functional role has still to be further elucidated. Furthermore, the exclusive presence of this keratin group in bichir, sturgeon and gar points to the close phylogenetic relationship of these ray- finned fish, an issue still under debate among taxonomists. Background from typeI/II heterodimers. The keratins are members of In vertebrates the cytoskeleton of epithelial cell types is the large multigene family of intermediate filament pro- typically reinforced by a specific set of type I and type II teins (IFproteins) of which they form by far the most com- keratins that assemble into 10 nm thick filaments formed plex group. In human, 53 of the hitherto nearly 70 Page 1 of 9 (page number not for citation purposes) Frontiers in Zoology 2007, 4:16 http://www.frontiersinzoology.com/content/4/1/16 identified IF protein genes code for keratins [1-4] that are Results and discussion expressed in tissue and developmental specific patterns. Novel type I keratin sequences from bichir, sturgeon and Without including human hair and nail forming keratins, gar the number of keratin genes found in teleost fish is com- Only recently we have discovered that a rather ancient and parably high, but in contrast to human and other tetrap- distant group of keratin-related sequences, the extracellu- ods, teleost fish possess a large excess of type I keratin larly secreted thread keratins TKα and TKγ, are not only genes [5-7]. By analysing the molecular evolution of kerat- present in hagfish (the assumedly most ancient vertebrate ins, as well as the evolution of their expression patterns in group), but also in lamprey, teleosts and amphibians. lower vertebrates, we want to further elucidate the sce- This provided major clues relating to keratin evolution in nario and probable evolutionary forces that led to this vertebrates, but also pointed to a more general role of this extraordinary variety of keratins in vertebrates. previously considered highly specific IF protein group in vertebrates [28]. By combination of RT-PCR experiments Our investigations of the keratin systems in lamprey, and cDNA library screening (for details see Methods), shark, trout, zebrafish, carp, goldfish and lungfish have so from sturgeon and gar we have now isolated one and from far revealed that type I and type II keratins are apparently bichir two cDNA sequences that, according to our phylo- present in all classes of vertebrates and that the various genetic analysis, code for members of another novel kera- keratins can generally be subdivided into the "E" keratins, tin group (Fig. 1, Table 1). The 1858 bp long cDNA clone expressed in epidermal keratinocytes and other stratified we isolated from the sturgeon cDNA library (abak14; epithelia, and those appearing in cells forming simple epi- [EMBL: AJ493259]) contains the complete coding thelia, thus named "S" keratins [8-19]. Nevertheless, our sequence for a type I keratin of 46759Da (431 amino data based on cDNA sequence analysis, followed by thor- acids) and a calculated pI of 5.1, which we now term ough phylogenetic analyses [13-18] as well as the studies AbaK14 (from Acipenser baeri keratin). However, the cor- based on the recently available genome data from man responding sequences we have so far obtained from bichir and teleost fish [1,2,5-7], strongly support the view of and gar are still incomplete. A 1369 bp long clone largely independent origins of the keratin genes found in (pseK14a; [EMBL: AM419452]) isolated from the bichir fish and man. According to our present data, solely the cDNA library encodes a type I keratin that we term typical "S" keratin pair K8 and K18 can at least be found PseK14a (Polypterus senegalus keratin). It still lacks a por- in all gnathostomian vertebrate groups, indicating the tion of its head encoding sequence in addition to its 5' unique and general importance of these "ancient" kerat- UTR. By RT-PCR using degenerate primers, from bichir we ins. In contrast to other vertebrates investigated so far, in additionally recovered a 908 bp long cDNA sequence modern teleost fish keratins, including K8 and K18, in (pseK14b; [EMBL: AM419453]), comprising almost the addition to their typical IF epithelial appearance show a complete rod encoding segment of a second K14 counter- widespread IF occurrence in mesenchymally derived cells part in this species (PseK14b). In addition, we found five and tissues, such as fibroblasts, chondrocytes and blood further incomplete cDNA clones that apparently encode vessel endothelia (for review see [11]). The latter in the different variants of PseK14a (not shown here). The latter non-teleost vertebrates usually do not express keratins but only slightly vary in DNA sequence, from 0.1 – 3.1% the type III IF protein vimentin [20-26]. To further trace (amino acid variance of 0.4 – 4.9%). In a similar way we the origin of the different "E" and "S" keratins as well as were also able to amplify a cDNA fragment encoding the the evolution of the mesenchymal keratin expression in rod domain of a K14 counterpart in gar, which we term teleosts, we have investigated the keratin systems in a LocK14 (from Lepisosteus oculatus keratin). By RACE-PCR bichir, a sturgeon and a gar that are believed to represent we additionally recovered its tail encoding sequence and the most ancient groups of the extant ray-finned fish. In 3' UTR. Its assembled sequence (lock14; [EMBL: the course of these studies, from all three species we AM419454]) overall comprises 1207 bp, but still lacks the obtained sequences that apparently belong to a novel complete head encoding segment in addition to the sec- branch of type I keratins, without counterparts in any tion coding for the first seven residues of the rod domain. other vertebrate group investigated so far, including the teleost fish. Here we present and discuss their sequences Subsequent mining of the available genome and EST data- as well as their phylogenetically relationships to the other bases for K14 counterparts in other vertebrates such as tel- members of the type I keratin subfamily, which may also eosts, amphibians, birds and mammals, so far has not yet provide clues to the early evolution of ray-finned fish. The yielded any matches, suggesting that this keratin group latter is still strongly debated among taxonomists, may only be present in the ancient groups of ray- finned whether on the basis of molecular or morphological data fish. We only found two matches encoding K14 of (for an overview see [27]). another sturgeon, notably Acipenser transmontanus (white sturgeon; [EMBL: DR975435, DR975694]), which both stem from a skin-derived cDNA library. Page 2 of 9 (page number not for citation purposes) Frontiers in Zoology 2007, 4:16 http://www.frontiersinzoology.com/content/4/1/16 SequenceFigure 1 comparison of K14 from bichir, sturgeon and gar Sequence comparison of K14 from bichir, sturgeon and gar. Multiple alignment of the keratin 14 (K14) sequences we obtained from bichir, sturgeon and gar.
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